Vagal-dependent nonlinear variability in the respiratory pattern of anesthetized, spontaneously breathing rats

Journal of Applied Physiology

Volumn 111, Issue 1, 2011, Pages 272-284

  Dhingra, R R ^a   Jacono, F J ^a,b   Fishman, M ^a   Loparo, K A ^c   Rybak, I A ^d   Dick, T E ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c Case Western Reserve University   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Breathing pattern variability; Entropy; K lliker fuse nucleus; Nonlinear dynamics; Vagus

Indexed keywords

AMINO ACID RECEPTOR BLOCKING AGENT; DIZOCILPINE MALEATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BREATHING; BREATHING MECHANICS; DRUG ANTAGONISM; DRUG EFFECT; ELECTROMYOGRAPHY; FEEDBACK SYSTEM; GENERAL ANESTHESIA; INNERVATION; LUNG; MALE; METABOLISM; MICROINJECTION; NONLINEAR SYSTEM; PERIODICITY; PHYSIOLOGY; PONS; RAT; SPRAGUE DAWLEY RAT; TIME; VAGOTOMY; VAGUS NERVE;

ANESTHESIA, GENERAL; ANIMALS; DIZOCILPINE MALEATE; ELECTROMYOGRAPHY; EXCITATORY AMINO ACID ANTAGONISTS; FEEDBACK, PHYSIOLOGICAL; LUNG; MALE; MICROINJECTIONS; MODELS, NEUROLOGICAL; NONLINEAR DYNAMICS; PERIODICITY; PONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RESPIRATION; RESPIRATORY MECHANICS; TIME FACTORS; VAGOTOMY; VAGUS NERVE;

EID: 79960263429     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.91196.2008     Document Type: Article

References (58)

1. 2 sensitivity of the complexity of phrenic neurograms in the piglet during early maturation. J Neural Eng 2:35-41, 2005. (Pubitemid 40771005)
2. Akay M. Influence of the vagus nerve on respiratory patterns during early maturation. IEEE Trans Biomed Eng 52:1863-1868, 2005. (Pubitemid 41578807)
3. Basmajian JV, Stecko G. A new bipolar electrode for electromyography. J Appl Physiol 17:849, 1962.
4. Bhattacharya J. Detection of weak chaos in infant respiration. IEEE Trans Syst Man Cybern B Cybern 31:637-642, 2001. (Pubitemid 32780094)
5. Burioka N, Cornelissen G, Halberg F, Kaplan DT, Suyama H, Sako T, Shimizu E. Approximate entropy of human respiratory movement during eye-closed waking and different sleep stages. Chest 123:80-86, 2003. (Pubitemid 36126717)
6. Burioka N, Suyama H, Sako T, Miyata M, Takeshima T, Endo M, Kurai J, Fukuoka Y, Takata M, Nomura T, Nakashima K, Shimizu E. Non-linear dynamics applied to human respiratory movement during sleep. Biomed Pharmacother 56, Suppl 2:370s-373s, 2002. (Pubitemid 35477697)
7. Caldirola D, Bellodi L, Caumo A, Migliarese G, Perna G. Approximate entropy of respiratory patterns in panic disorder. Am J Psychiatry 161:79-87, 2004. (Pubitemid 38419311)
8. Chen X, Chon KH, Solomon IC. Chemical activation of pre-Botzinger complex in vivo reduces respiratory network complexity. Am J Physiol Regul Integr Comp Physiol 288:R1237-R1247, 2005. (Pubitemid 40593707)
9. Coles SK, Dick TE. Neurones in the ventrolateral pons are required for post-hypoxic frequency decline in rats. J Physiol 497:79-94, 1996. (Pubitemid 26397674)
10. Dick TE. Artifactual averaged "twitch tension" waveforms resulting from synchronized activity: recording from feline diaphragmatic motor units. Neurosci Lett 114:57-62, 1990. (Pubitemid 20178267)
11. Dick TE, Shannon R, Lindsey BG, Nuding SC, Segers LS, Baekey DM, Morris KF. Pontine respiratory-modulated activity before and after vagotomy in decerebrate cats. J Physiol 586:5279-5279, 2008.
12. Dutschmann M, Herbert H. The Kolliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. Eur J Neurosci 24:1071-1084, 2006. (Pubitemid 44268138)
13. Dutschmann M, Morschel M, Reuter J, Zhang W, Gestreau C, Stettner G, Kron M. Postnatal emergence of synaptic plasticity associated with dynamic adaptation of the respiratory motor pattern. Respir Physiol Neurobiol 164:72-79, 2008.
14. Eldridge FL. Relationship between phrenic nerve activity and ventilation. Am J Physiol 221:535-543, 1971.
15. Eldridge FL, Gill-Kumar P. Central neural respiratory drive and afterdischarge. Respir Physiol 40:49-63, 1980. (Pubitemid 10149627)
16. Eldridge FL, Millhorn DE. Oscillation, gating, and memory in the respiratory control system. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, sect. 3, vol. II, pt. 1, chapt. 3, p. 93-113.
17. Ezure K, Tanaka I. Distribution and medullary projection of respiratory neurons in the dorsolateral pons of the rat. Neuroscience 141:1011-1023, 2006. (Pubitemid 44066669)
18. Feldman JL, Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7:232-242, 2006. (Pubitemid 43292468)
19. Fiamma MN, Straus C, Thibault S, Wysocki M, Baconnier P, Similowski T. Effects of hypercapnia and hypocapnia on ventilatory variability and the chaotic dynamics of ventilatory flow in humans. Am J Physiol Regul Integr Comp Physiol 292:R1985-R1993, 2007. (Pubitemid 46708556)
20. Fraser AM, Swinney HL. Independent coordinates for strange attractors from mutual information. Phys Rev A 33:1134-1140, 1986.
21. Fung ML, Wang WG, St. John WM. Involvement of pontile nmda receptors in inspiratory termination in rat. Respir Physiol 96:177-188, 1994. (Pubitemid 24135396)
22. Grassberger P, Procaccia I. Measuring the strangeness of strange attractors. Physica D 9:189-208, 1983.
23. Grippi MA, Pack AI, Davies RO, Fishman AP. Adaptation to reflex effects of prolonged lung inflation. J Appl Physiol 58:1360-1371, 1985. (Pubitemid 15033206)
24. Harris MB, Milsom WK. Apneusis follows disruption of NMDA-type glutamate receptors in vagotomized ground squirrels. Respir Physiol Neurobiol 134:191-207, 2003. (Pubitemid 36355853)
25. Hsieh YH, Siegel RE, Dick TE. Pontine GABAergic pathways: role and plasticity in the hypoxic ventilatory response. Respir Physiol Neurobiol 143:141-153, 2004. (Pubitemid 39425090)
26. Kaffashi F, Foglyano R, Wilson CG, Loparo KA. The effect of time delay on approximate and sample entropy calculations. Physica D 237:3069-3074, 2008.
27. Kaimakamis E, Bratsas C, Sichletidis L, Karvounis C, Maglaveras N. Screening of patients with Obstructive Sleep Apnea Syndrome using C4.5 algorithm based on non linear analysis of respiratory signals during sleep. Conf Proc IEEE Eng Med Biol Soc 2009:3465-3469, 2009.
28. Katz RL, Fink BR, Ngai SH. Relationship between electrical activity of the diaphragm and ventilation. Proc Soc Exp Biol Med 110:792-794, 1962.
29. Kelsen SG, Shustack A, Hough W. The effect of vagal blockade on the variability of ventilation in the awake dog. Respir Physiol 49:339-353, 1982. (Pubitemid 12027013)
30. Koo BB, Strohl KP, Gillombardo CB, Jacono FJ. Ventilatory patterning in a mouse model of stroke. Respir Physiol Neurobiol 172:129-135, 2010.
31. Lake DE, Richman JS, Griffin MP, Moorman JR. Sample entropy analysis of neonatal heart rate variability. Am J Physiol Regul Integr Comp Physiol 283:R789-R797, 2002. (Pubitemid 34951632)
32. Letellier C, Rabarimanantsoa H, Achour L, Cuvelier A, Muir JF. Recurrence plots for dynamical analysis of non-invasive mechanical ventilation. Philos Transact A Math Phys Eng Sci 366:621-634, 2008.
33. Lewis J, Bachoo M, Polosa C, Glass L. The effects of superior laryngeal nerve stimulation on the respiratory rhythm: phase-resetting and aftereffects. Brain Res 517:44-50, 1990. (Pubitemid 20207217)
34. Ling LM, Karius DR, Speck DF. Role of N-methyl-D-aspartate receptors in the pontine pneumotaxic mechanism in the cat. J Appl Physiol 76:1138-1143, 1994. (Pubitemid 24099952)
35. Mangin L, Leseche G, Duprey A, Clerici C. Ventilatory chaos is impaired in carotid atherosclerosis. PLoS One 6:e16297, 2010.
36. Okazaki M, Takeda T, Yamazaki H, Haji A. Synaptic mechanisms of inspiratory off-switching evoked by pontine pneumotaxic stimulation in cats. Neurosci Res 44:101-110, 2002. (Pubitemid 36158708)
37. Oku Y, Dick TE. Phase resetting of the respiratory cycle before and after unilateral pontine lesion in cat. J Appl Physiol 72:721-730, 1992.
38. Papaioannou VE, Chouvarda IG, Maglaveras NK, Pneumatikos IA. Study of multiparameter respiratory pattern complexity in surgical critically ill patients during weaning trials. BMC Physiol 11:2, 2010.
39. Pikkujamsa SM, Makikallio TH, Sourander LB, Raiha IJ, Puukka P, Skytta J, Peng CK, Goldberger AL, Huikuri HV. Cardiac interbeat interval dynamics from childhood to senescence: comparison of conventional and new measures based on fractals and chaos theory. Circulation 100:393-399, 1999. (Pubitemid 29362410)
40. Platisa MM, Gal V. Reflection of heart rate regulation on linear and nonlinear heart rate variability measures. Physiol Meas 27:145-154, 2006. (Pubitemid 43232105)
41. Richman JS, Moorman JR. Physiological time-series analysis using approximate entropy and sample entropy. Am J Physiol Heart Circ Physiol 278:H2039-H2049, 2000. (Pubitemid 30439218)
42. Rybak IA, Shevtsova NA, Paton JFR, Dick TE, St. John WM, Morschel M, Dutschmann M. Modeling the ponto-medullary respiratory network. Respir Physiol Neurobiol 143:307-319, 2004. (Pubitemid 39425102)
43. Rybak IA, Shevtsova NA, Paton JFR, Pierrefiche O, St. John WM, Haji A. Modelling respiratory rhythmogenesis: focus on phase switching mechanisms. Adv Exp Med Biol 551:189-194, 2004. (Pubitemid 40036670)
44. Sammon MP, Bruce EN. Vagal afferent activity increases dynamical dimension of respiration in rats. J Appl Physiol 70:1748-1762, 1991.
45. Schmidt M, Demoule A, Cracco C, Gharbi A, Fiamma MN, Straus C, Duguet A, Gottfried SB, Similowski T. Neurally adjusted ventilatory assist increases respiratory variability and complexity in acute respiratory failure. Anesthesiology 112:670-681, 2010.
46. Schreiber T, Schmitz A. Surrogate time series. Physica D 142:346-382, 2000.
47. Segers LS, Nuding SC, Dick TE, Shannon R, Baekey DM, Solomon IC, Morris KF, Lindsey BG. Functional connectivity in the pontomedullary respiratory network. J Neurophysiol 100:1749-1769, 2008.
48. Shannon CE. The mathematical theory of communication. 1963. MD Comput 14:306-317, 1997.
49. Siniaia MS, Young DL, Poon CS. Habituation and desensitization of the Hering-Breuer reflex in rat. J Physiol 523:479-491, 2000. (Pubitemid 30137654)
50. Song G, Poon CS. Functional and structural models of pontine modulation of mechanoreceptor and chemoreceptor reflexes. Respir Physiol Neurobiol 143:281-292, 2004. (Pubitemid 39425100)
51. Terrill PI, Wilson SJ, Suresh S, Cooper DM, Dakin C. Attractor structure discriminates sleep states: recurrence plot analysis applied to infant breathing patterns. IEEE Trans Biomed Eng 57:1108-1116, 2010.
52. Theiler J. Spurious dimension from correlation algorithms applied to limited time-series data. Phys Rev A 34:2427-2432, 1986.
53. Theiler J, Eubank S, Longtin A, Galdrikian B, Farmer JD. Testing for nonlinearity in time-series: the method of surrogate data. Physica D 58:77-94, 1992.
54. Thomas R. Deterministic chaos seen in terms of feedback circuits: analysis, synthesis, "labyrith chaos". Int J Bifurcat Chaos 9:1889-1905, 1999. (Pubitemid 129491327)
55. Veiga J, Faria RC, Esteves GP, Lopes AJ, Jansen JM, Melo PL. Approximate entropy as a measure of the airflow pattern complexity in asthma. Conf Proc IEEE Eng Med Biol Soc 1:2463-2466, 2010.
56. Weinreich G, Armitstead J, Teschler H. Pattern recognition of obstructive sleep apnoea and Cheyne-Stokes respiration. Physiol Meas 29:869-878, 2008.
57. White CE, Batchinsky AI, Necsoiu C, Nguyen R, Walker KP, 3rd, Chung KK, Wolf SE, Cancio LC. Lower interbreath interval complexity is associated with extubation failure in mechanically ventilated patients during spontaneous breathing trials. J Trauma 68:1310-1316, 2010.
58. Wysocki M, Fiamma MN, Straus C, Poon CS, Similowski T. Chaotic dynamics of resting ventilatory flow in humans assessed through noise titration. Respir Physiol Neurobiol 153:54-65, 2006. (Pubitemid 44131522)